2 Laboratory for Marine Ecology and Environmental Science, Qingdao National Laboratory for Marine Science and Technology, Qingdao 266071, China;
3 University of Chinese Academy of Sciences, Beijing 100049, China
There are more than 140 species of sea cucumbers have been classified in China, and about 20 species are edible according to historical records (Liao, 1997). Of these, the Japanese sea cucumber Apostichopus japonicus is the most economically important and valuable species. Apostichopus japonicus belongs to the Family Stichopodidae, Order Aspidochirotida, Class Holothuroidea in the Phylum Echinodermata (Liao, 1997; Zhao, 2015). Apostichopus japonicus is widely distributed in the Yellow Sea and the Bohai Sea in China, inhabiting shallow areas with reef substrates, abundant food supply, slow water currents, and no fresh water input (Liu, 2015).
According to historical records, Chinese people began eating sea cucumber in the Ming Dynasty, and it was listed as one of the top "eight sea treasures". Based on its health benefits, sea cucumber was considered the "ginseng of the sea" (Xia and Wang, 2015; Yang and Bai, 2015). In addition, sea cucumber has been believed to possess medicinal functions. The Supplement to the Compendium of Materia Medica in the Qing Dynasty reads, "The sea cucumber with black thorns produced in Liaodong is the best, which benefits to promote spermatogenesis and hematopoiesis" (Xia and Wang, 2015; Yang and Bai, 2015). Recently, biochemical analysis has revealed that the sea cucumber body wall is rich in nutrients and bioactive substances, such as amino acids, fatty acids, mucopolysaccharides and microelements (Li et al., 2006; Liu et al., 2011b; Xia and Wang, 2015; Yang and Bai, 2015). Economic development has improved food quality so that the Chinese people now enjoy a higher standard of living. Therefore, the market requirement and consumption of sea cucumbers has gradually increased in the past decade. As a result, the sea cucumber farming industry in China has been developing rapidly in order to meet the increasing market demand. According to data from the China Fishery Statistical Yearbook, the yield, mariculture area, and quantity of sea cucumber seedlings have greatly increased in recent years (Fisheries and Fisheries Administration Bureau of the Ministry of Agriculture, 1998–2017). By 2016, the mariculture area, yield and quantity of seedling were 21.8×104 hm2, 20.44×107 kg and 63.1 billion, respectively (Fisheries and Fisheries Administration Bureau of the Ministry of Agriculture, 2017). These data indicate that sea cucumber has become a key aquaculture species in China bringing significant economic benefits nationally (Fig. 1).2 CURRENT SITUATION OF SCIENCE AND TECHNOLOGY IN THE SEA CUCUMBER INDUSTRY 2.1 Basic biological research has received high attention
The life cycle of A. japonicus includes a pelagic auricularia larval stage, a benthic doliolaria stage, followed by a pentactula stage, which transitions into an early juvenile with ambulacral podia, and a final metamorphosis into the juvenile stage and the mature stage (Qiu et al., 2015).
Biological characteristics of A. japonicus include autolysis, aestivation, evisceration, and regeneration (Yang et al., 2014). Since A. japonicus is a typical temperate species, aestivation is employed as a strategy to adapt to high temperatures in summer. During aestivation, A. japonicus will stop feeding, become inactive, degrade the entire intestine, lose body mass, and reduce basal metabolism (Wang et al., 2015b). Evisceration is a defense mechanism for A. japonicus when they encounter chemical or physical stress. The missing organs and appendages can concurrently regenerate when conditions become favorable (Wang et al., 2015b). Likewise, autolysis by endogenous proteolytic enzymes in the muscle tissue takes place when A. japonicus is under environmental stress (Zhu et al., 2008).2.2 Aquaculture technology is developing rapidly
Sea cucumber aquaculture technology has been developing rapidly in China since the 1990s (Liu et al., 2015a). A series of effective aquaculture technologies based on sea cucumber biology have been constructed. These technologies include brood stock conditioning, larval rearing, juvenile rearing and brood stock rearing technologies, and several key technical indicators, including optimal water temperature, illumination intensity, salinity, stocking density and feed component have been determined in the last decade (Table 1). Several aquaculture models of adult A. japonicus also have been established (Fig. 2), such as bottom culture, pond culture, industrial culture, and cage culture methods (Zhang et al., 2015a).
Aquaculture facilities play an important role in improving the yield of sea cucumbers. Recently, specialized facilities including multilayered-plates reef systems, oyster-shell reef systems, and multilayered-concrete reef systems have been explored (Zhang et al., 2011a, 2015a, b). These artificial reefs can provide the suitable ecological conditions and abundant diet for optimum rearing of sea cucumbers in order to promote aquaculture success (Fig. 3).
Rearing sea cucumber varieties in culture has proven to be challenging due to the long period of first sexual maturity and the difficulty of genetic control of quantitative traits. To date, there are only two new varieties of A. japonicus (i.e. "Shuiyuan No. 1" and "Kongtong Island No. 1") in China (Liu et al., 2013; Yang et al., 2015). Both of these varieties show increased growth rates compared to natural populations (Table 4).
Over the past 30 years, sea cucumber aquaculture has become an important regional industry in the Liaodong Peninsula, the Shandong Peninsula and the Fujian Province. An indoor high-density hatchery of seedling cultivation and an outdoor polyculture of various economic species have been developed. An industrial chain of sea cucumber farming sites, primary processing and deep processing sites have been constructed in China.2.3 Health care function research is gradually developing
The health value of sea cucumbers as a traditional preferred food has been documented from ancient times. The studies of the pharmacological actions of active components in A. japonicus have been gradually uncovered, and some components have been used as drugs for clinical treatment.
Research on pharmacologically relevant compounds in sea cucumber over past 20 years, have discovered medicinal functions of polysaccharides, polypeptide and the protein holothurin (Zhao et al., 2011; Xia and Wang, 2015). Previous studies have found that such active compounds can promote hematopoietic ability and promote blood circulation to remove blood stasis (Yang and Bai, 2015). In addition, these compounds may also play an important role in anti-tumor, anti-oxidation, enhanced immunity, anti-aging and anti-fatigue functions in the immune system (Yang and Bai, 2015). Therefore, the medicinal value of A. japonicus has been emerging as an important aspect of the development of marine drugs. Continued research on A. japonicus shows great possibilities for potential immune dysfunction treatments in the future.3 PROBLEMS OF SEA CUCUMBER INDUSTRY
Although the development of the sea cucumber industry was rapid in recent years, the industry is now encountering a bottleneck. Several issues are demanding prompt solutions, such as the lack of basic biology research and abnormal climates in summer. The subjective and objective problems faced by the sea cucumber industry, may affect the sustainability of the aquaculture industry, the consumption market, and the functional sustainability of sea cucumbers providing potential health products.3.1 Biological concerns on biological studies
At present, research on the basic biology of A. japonicus is relatively weak and far behind the development of the A. japonicus aquaculture industry. For example, research on biological phenomena such as aestivation, autolysis, evisceration, regeneration, and albinism are still at the initial stages. However, the physiologic characteristics of sea cucumbers such as aestivation, evisceration, and autolysis have a close relationship with yield in aquaculture. Therefore, it is necessary to associate the industrial demands with the scientific payoffs to achieve sustainable development of the industry.
The technology of molecular marker-assisted selection in A. japonicus is just beginning, thus the guidelines of practice in the field of sea cucumber breeding have not been established (Xu et al., 2014). In addition, due to the limited understanding of basic biological characteristics, sea cucumber culture is plagued by disease throughout the farming process.
Compared to other aquatic animals such as shrimp, the diagnosis of A. japonicus diseases is ambiguous, and the real-time detection methods are still not known (Chen et al., 2015). Moreover, researches on pathogenic mechanisms and epidemic trends of A. japonicus are still unclear (Chen et al., 2015; Han et al., 2016).3.2 Germplasm degradation and lack of good varieties
Due to overfishing, habitat destruction, and other human factors, the safety of the sea cucumber germplasm resources is seriously being threatened. This may cause serious consequences. For example, the body size of a sexually mature individual is reducing, quantitative characteristic (i.e. numbers of thorn) is becoming single, the growth rate is becoming slow, and the resistant ability to changing environments is becoming poor. Germplasm degradation in sea cucumbers may become more serious in the future. On the one hand, due to the lack of habitat protection, wild resources will decline rapidly. On the other hand, due to increased use of bottom sowing culture pattern (Zhang et al., 2015a), unwanted genetic crosses may occur from hybridization with nearby native populations.
In addition, spring and autumn are the traditional fishing seasons for sea cucumbers. Spring is also the key season for gonadal development of sea cucumbers (Wang et al., 2015a). While generally, larger animals are easier to be found, this results in a large number of breeding individuals were caught.
Moreover, the brood stock used for artificial breeding is mainly collected from a cofferdam pond, in which the age of first sexual maturity is young (about two years) and the genetic diversity is low. Thus, the gamete quality is always difficult to control during artificial breeding (Liu et al., 2015b). Although the current scale of sea cucumber breeding is large, special varieties with high-quality economic characteristics are few compared with other aquaculture species, and the lack of improved varieties restricts the development of the sea cucumber farming industry.3.3 Environment stress resulting from global climate change
As a result of global climate change, the marine environment has shown a global trend of increasing water temperature and acidity with a corresponding decrease in dissolved oxygen. In recent years, sea cucumber aquaculture has responded negatively to these global changes, resulting in significant economic losses. For example, in the summers of 2013 and 2016, there was continuous hot weather in the coastal areas of northern China, resulting in large-scale death of sea cucumbers in the Shandong Peninsula.
Sea cucumbers are sensitive to the effects of environmental stress, including hyperthermia and acidification. Under these conditions, growth and metamorphosis rate are depressed, and the mortality rate increases in the larvae stage (Table 2). Growth is depressed in the juvenile stage (Table 2). For adults, high temperature can lead to aestivation, decreased metabolic activity, and depressed gonadal development (Table 2). In addition, acute heat stress causes rapid death in sea cucumbers, and the mortality rate is 77.2% in five days at 32℃ (Xu et al., 2014). Therefore, the scientific site selection of aquaculture ponds and the rational utilization of cooling and aerobic facilities are key strategies for the sea cucumber aquaculture industry to combat the effects of global climate change.3.4 Low efficiency of traditional aquaculture models
The current unit yield of A. japonicus in the traditional aquaculture model is approximately 937 kg/hm2 and the cultivation period of commercial A. japonicus is estimated at 2–3 years (Fisheries and Fisheries Administration Bureau of the Ministry of Agricultures, 1998–2017; Liu et al., 2015a). These poor numbers reflect the low efficiency of the traditional aquaculture models (Fig. 4).
The primary reason for this phenomenon is due to non-standard aquaculture techniques and extensive management. For example, due to the low quality of diet and inappropriate substrate materials, the deterioration of water quality in ponds could lead to a large-scale mortality rate of A. japonicus resulting in reduced production. In addition, A. japonicus as a benthic deposit feeder has the biological characteristics of low digestive ability and growth rate (Table 3). However, in most aquaculture regions, A. japonicus animals are cultivate separately. Therefore the upper and middle waters cannot be used fully. This contributes another critical reason for low aquaculture efficiency.3.5 Health care function urgently needs to be elucidated
The use of A. japonicus for marine drugs relies on nutrition facts of component polysaccharides, polypeptides and saponins in the body wall or gonadal tissues. While knowledge about the function of active substances such as cerebrosides is lacking, these components have been shown in other sea cucumber species to play an important role in the prevention of fatty liver (Xu et al., 2011).
Currently, in order to adapt to consumer demand, the processing capacity of sea cucumbers has been constantly improved (Mao et al., 2015). Processed products including instant food and capsules are in mass production in addition to traditional products (Fig. 5). However, due to the limitation of research method, and the complexity of sea cucumber active ingredients, there remain very few studies addressing the physiological and pharmacological regulation mechanisms of these compounds. Therefore, a comprehensive study of the health care functions in A. japonicus is relatively lagging behind the market demand. This may hinder A. japonicus sustainable development in the pharmaceutical, health and food industries.3.6 Food safety and market stability
Apostichopus japonicus is a rare seafood with high nutrition value that has gained great attention among consumers in the market. However, domestic food safety problems have been frequent in recent years. The phenomena of antibiotic residues and processing fraud have repeatedly occurred, seriously affecting the sustainable development of the A. japonicus market.
Food safety problems in A. japonicus occur in aquaculture and processing. Regarding aquaculture, the blanket use of antibiotics and additives damage the ecological balance of aquaculture water, and impair the physiological function of A. japonicus (Lv and Zhou, 2005; Liu et al., 2011a; The Xinhua News Agency, 2014; Han et al., 2016; Yang et al., 2017). In processing, several processing companies prepare dry A. japonicus with sodium hydroxide and syrup in order to reduce soaking time and increase the wet weight after soaking (Liu et al., 2010b; Wang et al., 2013; Luo et al., 2014). The addition of harmful preservatives, such as formaldehyde could cause serious food safety problems as well (Zhang et al., 2012; Li, 2013). Taken together, these factors will damage sustainable development of A. japonicus in coastal fish markets.4 DEVELOPMENT STRATEGY FOR THE SEA CUCUMBER INDUSTRY 4.1 Improving knowledge of biological characteristics based on the sea cucumber genome
In view of the weakness of basic biology research, the basic theory and application technology of A. japonicus biology should be strengthened. As a foundational basis of sea cucumber biology, the complete sequence of the sea cucumber genome should be efficiently used (Jo et al., 2017; Zhang et al., 2017). First, genomic data can provide information on the molecular mechanism of dormancy, body color control, and regeneration to better understanding lifehistory strategies in A. japonicus. In addition, genomic data can also be used for promoting high-quality traits including body thorns, heat-resistance, diseaseresistance, and fast growth in A. japonicus.
Moreover, in order to better control diseases during aquaculture, disease-related immune genes in the A. japonicus genome are necessary. These genes could help explore pathogenesis, produce new drugs, and develop antiviral vaccines in view of molecular mechanism. Disease research should be closely associated with aquaculture practices, so that largescale infectious disease can be controlled in culture further guaranteeing sustainable development of A. japonicus in the aquaculture industry.4.2 Improving aquaculture technology based on behavioral studies
Challenges in sea cucumber aquaculture include selection of appropriate farming sites, uncontrollable distribution of farming animals, low recapture rate of farming animals, and low efficiency of fishing style (Fig. 6). Research concerned with the behavioral ecology of sea cucumbers can effectively address the problems mentioned above.
Behaviors of sea cucumbers include movement, feeding, and habitat selection (Pan et al., 2015; Sun et al., 2015; Ru et al., 2017). Researchers are paying attention to the behavior of sea cucumbers due to the significant scientific value of this information poses for aquaculture. For example, understanding feeding behavior and digestive physiology, the feeding rhythms (peaks at 02:00–04:00) of sea cucumbers can be determined (Sun et al., 2015). This information can provide guidance for more efficient feeding strategies for factory farming. Moreover, behavioral data also can provide theoretical support for the development of aquaculture and trapping facilities (Zhang et al., 2011a).4.3 Improving aquaculture varieties based on modern breeding technology
Directional selection of wild populations and improvement of high-quality economic traits, using modern biological technology and genetic principles, provide crucial support for the sea cucumber aquaculture industry. For example, the filial generation, which was a hybridization between Russian population and Chinese population of sea cucumbers, showed an obvious increase in growth rate and survival rate (Table 4). Other traits, including white color, purple color, and six rows of papilla are constructed now (Chang et al., 2011; Bai et al., 2015). These high-quality strains will lay the foundation for the diversification of aquaculture species (Fig. 7).4.4 Aquaculture model optimization based on ecological principals
Development of co-culture patterns is beneficial for the efficient use of limited aquaculture space, the increase of diet utilization and decrease of output of aquaculture waste, as well as increasing economic benefits. Apostichopus japonicus, as a typical benthic deposit feeder, can effectively reduce the organic content in aquaculture systems (Yuan et al., 2015b; Zamora et al., 2018). For example, the development of tridimensional aquaculture patterns, such the polyculture of sea cucumber with shellfish, abalone, jellyfish, sea urchin and fish can significantly improve the utilization efficiency of water resources (Yuan et al., 2015b). In addition, sea cucumbers can transform biological sediments in polyculture systems into body tissues at rates of 0.8–4.6 and 0.3–0.8 mg/(g·d) for carbon and nitrogen, respectively (Yuan et al., 2015b). Another example, the interactive polyculture of sea cucumber and shrimp can harvest extra shrimp (150 kg/ hm2) in A. japonicus aestivation (He et al., 2008).
The use of modern aquaculture facilities can significantly improve the aquaculture density, and thus significantly improve the unit yield and aquaculture efficiency (Lin and Zhang, 2015). Based on the biological characteristics of A. japonicus, and the shallow water environment in China, environmentally friendly facilities such as oystershell reefs can not only increase sea cucumber aquaculture efficiency to 20 ind./m2, but also provide habitats for other invertebrates. Such a system will have positive effects on marine resources and habitat rehabilitation (Zhang et al., 2015b).4.5 Establishing a traceable system of food safety and quality
The ultimate quality of sea cucumber products can be affected by seedling production, aquaculture, processing and preservation (Zhang et al., 2014a). Therefore, it is necessary to establish a sophisticated traceable system in order to guarantee food safety of sea cucumbers over the entire production scheme. Every level of production should participate in the construction of the quality control system, from sea cucumber aquaculture, to processing and marketing.
Moreover, it is necessary to establish the national standard of sea cucumber product safety, standardize the production of dried sea cucumbers and the order of market competition. Efforts such as these will promote a healthy and sustainable sea cucumber market.
In order to address consumer concerns about the abuse of antibiotics, drug residue detection should be strengthened. In addition, research on highly efficient and green antibiotics should be the focus of current work. The use of Chinese herbal preparations and microbial preparations to prevent and treat diseases should be widely promoted. For example, the addition of 3% (w/w) astragalus polysaccharide in the diet can improve immunity, enhance resistance to pathogens and promote growth by 30.03% of A. japonicus (Sun et al., 2009; Wang et al., 2009).4.6 Exploring health care functions based on modern medical technology
With the improved living standard of Chinese people, consumers pay more attention to the health care functions of A. japonicus. Therefore, future studies should combine modern marine biotechnology and modern medical technology to evaluate the health care functions of sea cucumbers more comprehensively and scientifically (Xia and Wang, 2015). Exploring the pharmacological mechanisms of active ingredients from A. japonicus should be another important area of focus.
Regarding extraction of active substances from A. japonicus, future studies should combine the advanced technology of modern physical and chemical purification methods, and establish the industrial standard of the purification process to ensure the quality and purification efficiency of active substances. In addition, research on the genome of A. japonicus can provide the scientific basis for the development of new functional food and health products. For example, future studies can use known gene sequences to manufacture synthetic substitutes of active compounds. In this way, the health care products from A. japonicus can be produced on a large scale to advance a broad application of prospects.5 DATA AVAILABILITY STATEMENT
The data that support the findings of this study are available in the China Fishery Statistical Yearbook (Fisheries and Fisheries Administration Bureau of the Ministry of Agriculture, 1998–2017).6 ACKNOWLEDGEMENT
We are grateful to XU Qinzeng, JIANG Lingxu, ZHANG Chuantao, LI Jiao, QIU Tianlong and YANG Jianmin for providing the photographs. And we are also grateful to WU Yi for her excellent work in image editing.
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